Association of Superior Oblique Muscle Volumes with the Presence or Absence of the Trochlear Nerve on High-Resolution MR Imaging in Congenital Superior Oblique Palsy

Discussion

In this study, a strong relation was found between the quantitative evaluation of SO volume and the presence or absence of the trochlear nerve in patients with clinically diagnosed congenital SOP. The main findings are as follows: First, the cross-sectional area and volume of the paretic side SO were significantly smaller compared with the normal side in the absent group of congenital SOP. Second, the ratio of paretic/normal side SO volume and area near the optic nerve–globe junction was ≤0.75 in patients with SOP without the trochlear nerve. Finally, SO area and volume of the contralateral normal side were larger in both groups of patients with congenital SOP than in controls.

Hypoplasia of the ipsilateral SO has been the major finding on MR imaging of patients with congenital or idiopathic SOP.^{1⇓⇓⇓–5} However, the extent of SO hypoplasia compared with the contralateral side varied widely from 0% to 100% in previous reports.^1⇓–3 Sato¹ stated that in congenital SOP, there were 2 peaks in the distribution of the percentage volume of muscle size compared with the contralateral normal side: one between 20% and 40% and the other between 90% and 100%. These 2 groups correspond well to the absent group and present group of congenital SOP in our study because the mean ratio of paretic/normal side SO volume was 43% in the absent group and 103% in the present group—that is, the paretic side SO volume was abnormally small only in the patients with an absent trochlear nerve. As we have demonstrated in our previous study, the 2 groups classified by the absence or presence of the trochlear nerve in congenital SOP account for the 2 main etiologies of congenital SOP.³ The first is based on abnormalities of the muscle and its innervations associated with SO hypoplasia and trochlear nerve absence and the other is based on the pathologic features of the tendon or heterotopic muscle pulleys.^1,13

The ratio of paretic/normal side SO volume and SO area at the optic nerve–globe junction demonstrated excellent predictability for trochlear nerve absence. On the basis of the quantitative results of our study, we may expect that patients with congenital SOP with a significant SO hypoplasia of ≤75% compared with the contralateral normal side are likely to have trochlear nerve absence. As the coronal image plane moved anterior from the optic nerve–globe junction (plane +2, +4), however, the predictability of the SO area and the ratio of paretic/normal side SO area significantly decreased compared with the optic nerve–globe junction (plane “0”) or posterior planes (plane −2, −4) (Fig 3)—that is, SO hypoplasia of the paretic side compared with the normal side was less apparent in the anterior planes. This difference can be inferred from the fact that the anterior part of the SO ends in a rounded tendon, which acts in a fibrocartilaginous pulley attached to the trochlear fovea of the frontal bone. On the other hand, the predictability of the posterior planes (−2, −4) was also lower than that of the optic nerve–globe junction, probably owing to the fusiform structure of the SO. Considering the individual variations in orbital depth and position of the SO muscle/tendon transition, the best plane for evaluating SO hypoplasia should be adjusted to the image plane having the greatest cross-sectional area of the SO.¹⁴ Previous studies have shown that despite the individual variation, the coronal section at the nearest location posterior to the globe and optic nerve junction may be suitable for evaluating hypoplasia of the extraocular muscles.^2,7 This finding was consistent with our results, because SO hypoplasia and associated trochlear nerve absence were best predicted by the cross-sectional area of the SO near the optic nerve–globe junction. The SO volume and the sum of the SO areas at 5 planes also demonstrated good predictability of SO hypoplasia and trochlear nerve absence. However, the cross-sectional area of the SO in the plane nearest the optic nerve–globe junction was sufficient for this purpose.

The SO area and volume of the contralateral normal side were larger in patients with congenital SOP than in controls. Although it has been reported that the average maximum SO cross-section for the fellow eyes was not significantly different from those in healthy controls,¹⁴ more recent reports showed a larger size and supernormal contractility of the normal contralateral SO compared with that in controls in patients with SOP.⁷ Contralateral SO hypertrophy corresponds to the clinical finding of contralateral overdepression in adduction and may be suggestive of an adaptive change, change of fiber type distribution, or innervational change.⁷ On the other hand, because we did not control fixation during imaging, variable positions of the eyeball could have affected the muscle size. The normal fellow eye of patients with congenital SOP may show a relatively downward displacement compared with that in healthy controls, and downward displacement leads to a larger cross-section of the SO and inferior rectus muscle.¹⁴

The results of our study should be limited to congenital SOP and cannot be applied to acquired or idiopathic SOP. Acquired SOP may also show variable atrophy of the SO muscle, as in the absent group of congenital SOP.¹⁵ A significant volume loss of the SO muscles in acquired trochlear nerve palsies has also been reported, and the nerve may also “regress” and die back, becoming severely hypoplastic.¹⁶ The trochlear nerve may regress or become hypoplastic after perinatal injury or, in older patients, from diabetes or a developing small mass along the tentorial incisura.¹⁷ Thus, just because the volume of the SO is significantly decreased, we cannot conclude that the etiology is from nerve absence. In addition, variable degrees of SO muscle atrophy can be found in both congenital and acquired cases with no significant difference in the appearance of the SO muscle between acquired and congenital SOP groups.¹⁵ Moreover, the Bielschowsky head tilt test is not specific and may lead to erroneous results.¹⁷ The presence of large vertical fusional amplitudes does not necessarily imply a congenital etiology because vertical fusional vergence may increase in adults within weeks or months after an acquired vertical strabismus.¹⁷ Therefore, the diagnosis of congenital or acquired SO palsy cannot be concluded solely by imaging or ocular motor examination, but a thorough history and clinical examination are necessary. In these cases, the clinical features are quite different, such as the age of onset, facial asymmetry, and trochlear nerve status. Congenital SOP would be diagnosed mostly in early childhood with significant head tilt or with facial asymmetry in adulthood. In patients with severe SO muscle atrophy, trochlear nerve imaging with high-resolution MR imaging revealing an absent nerve would favor a congenital etiology, while a relatively normal trochlear nerve would suggest acquired SOP.³

There are certain limitations to our study. First, this is a retrospective study, not free of unintended confounding issues and a bias toward selecting severely affected patients in a tertiary referral center. Second, patients were excluded if they had poor-quality MR images: motion artifacts, obscured SO margins, or SO tendons extending more posteriorly than the optic nerve–globe junction, applicable to 3 patients of the total 162 study participants. Third, variable positions of the eyeball could have affected the muscle size. MR imaging sequences with higher resolutions by using fixation targets during imaging could overcome these problems.